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. 1985 Sep;49(3):664–669. doi: 10.1128/iai.49.3.664-669.1985

C1q, a subunit of the first component of complement, enhances binding of plasma fibronectin to bacteria.

J M Sorvillo, E Pearlstein
PMCID: PMC261237  PMID: 3875560

Abstract

The interaction of plasma fibronectin with C1q of the complement system has been demonstrated in the past several years. In addition, the antibody-independent binding of C1q to bacteria, as well as the binding of plasma fibronectin to bacteria, is well documented. This study examines whether the binding of C1q to bacteria enhances the interaction of C1q and bacteria with plasma fibronectin. Highly purified 125I-C1q bound to several species of bacteria in the absence of antibody. The binding of 125I-C1q to bacteria was saturable and specific since the addition of unlabeled C1q inhibited binding while the presence of bovine serum albumin did not. Bacteria which had been pretreated with either buffer or unlabeled C1q were tested for their ability to bind 125I-fibronectin. When bacteria were preincubated with buffer, Staphylococcus aureus bound fivefold more 125I-fibronectin than did Escherichia coli. However, preincubation of E. coli with C1q increased the binding of 125I-fibronectin by up to 20-fold, whereas pretreatment of S. aureus with C1q increased fibronectin binding by only twofold. These results were confirmed by immunoblotting studies which demonstrated the presence of C1q, as well as an increase in fibronectin antigens on the C1q-treated bacteria as compared with the level of fibronectin on buffer-treated bacteria. In addition, preincubation of 3H-labeled bacteria with C1q enhanced their attachment to fibronectin-coated surfaces but not to albumin-coated surfaces. The biological consequences of these observations are discussed.

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Selected References

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  1. Abraham S. N., Beachey E. H., Simpson W. A. Adherence of streptococcus pyogenes, Escherichia coli, and Pseudomonas aeruginosa to fibronectin-coated and uncoated epithelial cells. Infect Immun. 1983 Sep;41(3):1261–1268. doi: 10.1128/iai.41.3.1261-1268.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Betz S. J., Isliker H. Antibody-independent interactions between Escherichia coli J5 and human complement components. J Immunol. 1981 Nov;127(5):1748–1754. [PubMed] [Google Scholar]
  3. Bing D. H., Almeda S., Isliker H., Lahav J., Hynes R. O. Fibronectin binds to the C1q component of complement. Proc Natl Acad Sci U S A. 1982 Jul;79(13):4198–4201. doi: 10.1073/pnas.79.13.4198. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Calcott M. A., Müller-Eberhard H. J. C1q protein of human complement. Biochemistry. 1972 Aug 29;11(18):3443–3450. doi: 10.1021/bi00768a018. [DOI] [PubMed] [Google Scholar]
  5. Clas F., Golecki J. R., Loos M. Electron microscopic study showing antibody-independent binding of C1q, a subcomponent of the first component of complement, to serum-sensitive salmonellae. Infect Immun. 1984 Sep;45(3):795–797. doi: 10.1128/iai.45.3.795-797.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Clas F., Loos M. Antibody-independent binding of the first component of complement (C1) and its subcomponent C1q to the S and R forms of Salmonella minnesota. Infect Immun. 1981 Mar;31(3):1138–1144. doi: 10.1128/iai.31.3.1138-1144.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cooper N. R. Activation and regulation of the first complement component. Fed Proc. 1983 Jan;42(1):134–138. [PubMed] [Google Scholar]
  8. Cooper N. R., Jensen F. C., Welsh R. M., Jr, Oldstone M. B. Lysis of RNA tumor viruses by human serum: direct antibody-independent triggering of the classical complement pathway. J Exp Med. 1976 Oct 1;144(4):970–984. doi: 10.1084/jem.144.4.970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Fröman G., Switalski L. M., Faris A., Wadström T., Hök M. Binding of Escherichia coli to fibronectin. A mechanism of tissue adherence. J Biol Chem. 1984 Dec 10;259(23):14899–14905. [PubMed] [Google Scholar]
  10. Hynes R. O., Yamada K. M. Fibronectins: multifunctional modular glycoproteins. J Cell Biol. 1982 Nov;95(2 Pt 1):369–377. doi: 10.1083/jcb.95.2.369. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Ingham K. C., Brew S. A., Miekka S. I. Interaction of plasma fibronectin with gelatin and complement C1q. Mol Immunol. 1983 Mar;20(3):287–295. doi: 10.1016/0161-5890(83)90068-8. [DOI] [PubMed] [Google Scholar]
  12. Kuusela P. Fibronectin binds to Staphylococcus aureus. Nature. 1978 Dec 14;276(5689):718–720. doi: 10.1038/276718a0. [DOI] [PubMed] [Google Scholar]
  13. Kuusela P., Vartio T., Vuento M., Myhre E. B. Binding sites for streptococci and staphylococci in fibronectin. Infect Immun. 1984 Aug;45(2):433–436. doi: 10.1128/iai.45.2.433-436.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. LEPOW I. H., NAFF G. B., TODD E. W., PENSKY J., HINZ C. F. Chromatographic resolution of the first component of human complement into three activities. J Exp Med. 1963 Jun 1;117:983–1008. doi: 10.1084/jem.117.6.983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  16. Leist-Welsh P., Bjornson A. B. Immunoglobulin-independent utilization of the classical complement pathway in opsonophagocytosis of Escherichia coli by human peripheral leukocytes. J Immunol. 1982 Jun;128(6):2643–2651. [PubMed] [Google Scholar]
  17. Loos M., Wellek B., Thesen R., Opferkuch W. Antibody-independent interaction of the first component of complement with Gram-negative bacteria. Infect Immun. 1978 Oct;22(1):5–9. doi: 10.1128/iai.22.1.5-9.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Menzel E. J., Smolen J. S., Liotta L., Reid K. B. Interaction of fibronectin with C1q and its collagen-like fragment (CLF). FEBS Lett. 1981 Jun 29;129(1):188–192. doi: 10.1016/0014-5793(81)80787-9. [DOI] [PubMed] [Google Scholar]
  19. Mosher D. F., Proctor R. A. Binding and factor XIIIa-mediated cross-linking of a 27-kilodalton fragment of fibronectin to Staphylococcus aureus. Science. 1980 Aug 22;209(4459):927–929. doi: 10.1126/science.7403857. [DOI] [PubMed] [Google Scholar]
  20. Pearlstein E., Gold L. I., Garcia-Pardo A. Fibronectin: a review of its structure and biological activity. Mol Cell Biochem. 1980 Feb 8;29(2):103–128. doi: 10.1007/BF00220304. [DOI] [PubMed] [Google Scholar]
  21. Pearlstein E., Sorvillo J., Gigli I. The interaction of human plasma fibronectin with a subunit of the first component of complement, C1q. J Immunol. 1982 May;128(5):2036–2039. [PubMed] [Google Scholar]
  22. Porter R. R., Reid K. B. Activation of the complement system by antibody-antigen complexes: the classical pathway. Adv Protein Chem. 1979;33:1–71. doi: 10.1016/s0065-3233(08)60458-1. [DOI] [PubMed] [Google Scholar]
  23. Proctor R. A., Hamill R. J., Mosher D. F., Textor J. A., Olbrantz P. J. Effects of subinhibitory concentrations of antibiotics on Staphylococcus aureus interactions with fibronectin. J Antimicrob Chemother. 1983 Oct;12 (Suppl 100):85–95. doi: 10.1093/jac/12.suppl_c.85. [DOI] [PubMed] [Google Scholar]
  24. Proctor R. A., Mosher D. F., Olbrantz P. J. Fibronectin binding to Staphylococcus aureus. J Biol Chem. 1982 Dec 25;257(24):14788–14794. [PubMed] [Google Scholar]
  25. Proctor R. A., Prendergast E., Mosher D. F. Fibronectin mediates attachment of Staphylococcus aureus to human neutrophils. Blood. 1982 Apr;59(4):681–687. [PubMed] [Google Scholar]
  26. Reid K. B., Porter R. R. The proteolytic activation systems of complement. Annu Rev Biochem. 1981;50:433–464. doi: 10.1146/annurev.bi.50.070181.002245. [DOI] [PubMed] [Google Scholar]
  27. Simpson W. A., Beachey E. H. Adherence of group A streptococci to fibronectin on oral epithelial cells. Infect Immun. 1983 Jan;39(1):275–279. doi: 10.1128/iai.39.1.275-279.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Simpson W. A., Hasty D. L., Mason J. M., Beachey E. H. Fibronectin-mediated binding of group A streptococci to human polymorphonuclear leukocytes. Infect Immun. 1982 Aug;37(2):805–810. doi: 10.1128/iai.37.2.805-810.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Sorvillo J., Gigli I., Pearlstein E. Fibronectin binding to complement subcomponent C1q. Localization of their respective binding sites. Biochem J. 1985 Feb 15;226(1):207–215. doi: 10.1042/bj2260207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Sorvillo J., Gigli I., Pearlstein E. Requirements for the binding of human plasma fibronectin to the C1q subunit of the first component of complement. J Immunol. 1983 Sep;131(3):1400–1404. [PubMed] [Google Scholar]
  31. Storrs S. B., Kolb W. P., Olson M. S. C1q binding and C1 activation by various isolated cellular membranes. J Immunol. 1983 Jul;131(1):416–422. [PubMed] [Google Scholar]
  32. Switalski L. M., Rydén C., Rubin K., Ljungh A., Hök M., Wadström T. Binding of fibronectin to Staphylococcus strains. Infect Immun. 1983 Nov;42(2):628–633. doi: 10.1128/iai.42.2.628-633.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Tenner A. J., Cooper N. R. Stimulation of a human polymorphonuclear leukocyte oxidative response by the C1q subunit of the first complement component. J Immunol. 1982 Jun;128(6):2547–2552. [PubMed] [Google Scholar]
  34. Tenner A. J., Lesavre P. H., Cooper N. R. Purification and radiolabeling of human C1q. J Immunol. 1981 Aug;127(2):648–653. [PubMed] [Google Scholar]
  35. Tenner A. J., Ziccardi R. J., Cooper N. R. Antibody-independent C1 activation by E. coli. J Immunol. 1984 Aug;133(2):886–891. [PubMed] [Google Scholar]
  36. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Van de Water L., Destree A. T., Hynes R. O. Fibronectin binds to some bacteria but does not promote their uptake by phagocytic cells. Science. 1983 Apr 8;220(4593):201–204. doi: 10.1126/science.6338594. [DOI] [PubMed] [Google Scholar]
  38. Verbrugh H. A., Peterson P. K., Smith D. E., Nguyen B. Y., Hoidal J. R., Wilkinson B. J., Verhoef J., Furcht L. T. Human fibronectin binding to staphylococcal surface protein and its relative inefficiency in promoting phagocytosis by human polymorphonuclear leukocytes, monocytes, and alveolar macrophages. Infect Immun. 1981 Sep;33(3):811–819. doi: 10.1128/iai.33.3.811-819.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Wright S. D., Craigmyle L. S., Silverstein S. C. Fibronectin and serum amyloid P component stimulate C3b- and C3bi-mediated phagocytosis in cultured human monocytes. J Exp Med. 1983 Oct 1;158(4):1338–1343. doi: 10.1084/jem.158.4.1338. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Ziccardi R. J., Cooper N. R. Active disassembly of the first complement component, C-1, by C-1 inactivator. J Immunol. 1979 Aug;123(2):788–792. [PubMed] [Google Scholar]

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